Stereophotogrammetric approaches to multi-segmental kinematics of the thoracolumbar spine: a systematic review

Background Spine disorders are becoming more prevalent in today’s ageing society. Motion abnormalities have been linked to the prevalence and recurrence of these disorders. Various protocols exist to measure thoracolumbar spine motion, but a standard multi-segmental approach is still missing. This study aims to systematically evaluate the literature on stereophotogrammetric motion analysis approaches to quantify thoracolumbar spine kinematics in terms of measurement reliability, suitability of protocols for clinical application and clinical significance of the resulting functional assessment. Methods Electronic databases (PubMed, Scopus and ScienceDirect) were searched until February 2022. Studies published in English, investigating the intersegmental kinematics of the thoracolumbar spine using stereophotogrammetric motion analysis were identified. All information relating to measurement reliability; measurement suitability and clinical significance was extracted from the studies identified. Results Seventy-four studies met the inclusion criteria. 33% of the studies reported on the repeatability of their measurement. In terms of suitability, only 35% of protocols were deemed suitable for clinical application. The spinous processes of C7, T3, T6, T12, L1, L3 and L5 were the most widely used landmarks. The spine segment definitions were, however, found to be inconsistent among studies. Activities of daily living were the main tasks performed. Comparable results between protocols are however still missing. Conclusion The literature to date offers various stereophotogrammetric protocols to quantify the multi-segmental motion of the thoracolumbar spine, without a standard guideline being followed. From a clinical point of view, the approaches are still limited. Further research is needed to define a precise motion analysis protocol in terms of segment definition and clinical relevance.

following surgery ranging between 10 and 46% [7] due to instrumentation failure or sagittal imbalance [7,10]. These disorders include a wide range of clinical and radiographical characteristics [6]. However, current research suggests that movement abnormalities impact the prevalence of spinal disorders and the recurrence of the disease following treatment [11,12], hence the need for a better understanding of spine kinematics to improve treatment decisions and outcomes [13,14].
Different quantification methods are available to quantitatively characterize spine kinematics and posture. i) Spinal alignment angles in the frontal and sagittal planes are quantified in static conditions by means of imaging techniques [15], such as X-rays, CT or MRI scans [9,15,16]. These angles are commonly used in clinical practice to support diagnosis, surgical planning, and pre-and post-intervention assessment [9], but do not provide any characterization of spine function in dynamic conditions [16]. Static measurements are also affected by the limited repeatability of the measurements [15] with up to 20% change in lumbar lordosis values in subjects inter-session [17]. Additionally, depending on the spine pathology, imaging techniques are highly affected by lower levels of sensitivity, specificity and an increased rate of false positives with MRI being the most specific and sensitive test for LBP [18]. ii) Intervertebral 3D kinematics can be quantified using video-fluoroscopy [15,16].This technique is highly accurate, detecting intervertebral ROM with a measurement error varying between 0.32° and 0.52° in the coronal and sagittal plane, respectively [19], but it is not exploited in clinical practice due to the small imaging volume preventing the analysis of spine segments, and due to the critical ionizing radiations exposure [20]. iii) Spine 3D angles can be quantified non-invasively using stereophotogrammetric motion analysis [21] without field of view limitations, allowing also for the assessment during daily living activities [22,23], but can potentially be affected by significant experimental errors [24]. An overview of stereophotogrammetric motion analysis of the spine can be seen in Fig. 1.
Stereophotogrammetric motion analysis is extensively used for the assessment of body segment kinematics during gait and other functional tasks [25,26]; although specific protocols and biomechanical models used for the assessment can differ [27]. Body segments (i.e. trunk, pelvis and limb segments) and joint definitions are consistent among protocols [28,29], while, for spine kinematics, a standard multi-segmental approach is still missing [24,30].
To assess thoracolumbar spine kinematics in an everyday clinical setting, reliable, clinically significant, and comparable data need to be reported by spinal motion protocols to provide a functional assessment of each spine segment and supply clinicians with a tool to characterize thoracolumbar kinematics changed by different pathologies. To achieve this, a set of standards and guidelines need to be agreed upon with recommendations on the motion tasks to carry out, optimal segment definitions, data to be generated and requirements for a protocol to be suitable for clinical application. Some previous review papers assessing spine motion analysis partially covered the clinical significance of thoracolumbar spine kinematic protocols [24,[31][32][33][34] or provided methodological information on the protocols available [24,25]. However, this review aims to provide a complete assessment of available protocols in terms of 1) reliability of the measurement, 2) suitability of the protocol for clinical application and 3) clinical significance of the reported results to unravel comparable outcomes between the protocols found and ultimately provide recommendations on the standards needed for thoracolumbar motion analysis. As LBP and ASD are pathologies that affect the thoracolumbar spine [1,35], motion protocols of only the cervical spine were not included in this review.
The review uncovers information relating to the measurement repeatability and accuracy approaches, number of markers used, segment definitions, degrees of freedom assessed, motion analysis system used, task choice, number of participants included, main measurements reported, pathologies assessed, and clinical findings.

Methods
This systematic review was conducted in accordance with the PRISMA statement [36].

Study selection and research criteria
Article search was completed on the 7 th of February 2022 on Scopus, PubMed, and Science Direct databases. The research keywords were customised to match each of the databases. Details of the research strings on each of the databases could be seen in Table 1. To understand the effect of LBP and ASD on the motion of the spine studies focusing solely on the cervical spine were excluded.
The outcomes of the searches on the different databases were merged into a single list.
Studies were included in the review if they met the following inclusion criteria: 1) journal papers written in English, 2) assessing the intersegmental motion of the thoracolumbar spine, 3) using stereophotogrammetric motion analysis, Articles passing inclusion criteria were retained as fulltext documents.

Quality assessment
The quality of the included studies was assessed by one reviewer using a customised quality assessment questionnaire including 19 questions. Questions 1-12 were designed to appraise the general quality of the studies in terms of study design and reproducibility of the method used. Questions 13 to 19 were specifically designed to assess the reliability of the measurement approach, the suitability of the approach to be used in a clinical setting and the clinical significance of the measurement. Quality assessment questions are listed in Table 2.
Each question was scored on a three-level basis: 2 = yes, 1 = limited detail, 0 = no, for an overall score of up to 38 possible points for each article. Bishop et al. [37] rating score was used to classify studies by their quality: high quality was associated to articles with a score higher than 80% (31/38), medium quality articles had a score between 51 and 79% (19-30/38) while low quality was associated with a score lower than 50% (18/38).

Data extraction
A standardised extraction form was used by one reviewer to identify and report relevant information from each study. The extraction form points are listed in Table 3.
The study details extracted could be divided into three categories: reliability of the measurement (points 1 to 3), suitability of the approach to be used in a clinical setting (points 4 to 9) and the clinical significance of the results reported (points 10 to 12). Some of the data extracted were related to more than one category; this was the case for points 4,5,6,8 which related to both the repeatability and suitability of the measurement, points 9 and 10 related to both the suitability of the measurement and the clinical significance of the reported results. Since none of the studies assessed in this review reported on the suitability of the measurement to be used in a clinical setting in terms of time needed to attach the markers and the ease of use of their data processing approach by clinicians, the number of markers used, segments defined, and degrees of freedom studied were reported instead to determine this suitability. Studies using the same protocol as previous ones were grouped into a separate list.

Data acquisition and research strategy
The selection process identified a total of 10,465 records, resulting in 8937 after duplicate removal. After screening titles and abstracts, 8827 studies were excluded as they were deemed irrelevant for the purposes of this review. Inclusion criteria were applied to 110 full-text articles. Seventy-four papers were found to match the inclusion criteria established while 36 studies were excluded as these did not report information on their marker setup, did not use an optoelectronic technique or defined the spine as one moving segment. The process for study selection is shown in the PRISMA flow chart (Fig. 2). Of
The number of articles answering yes to the quality assessment questions could be seen in Fig. 4.
The details and study characteristics obtained from the extraction form of the 74 articles reviewed could be found in Tables 4 and 5.
3) Did the description of the method used, allow for a replication of the measurement? 4) Is the motion analysis system and setup described?  sensors along with passive markers to cross-check the values generated by both systems [84,93]. Two studies compared the kinematic variables collected from participants to those collected from markers placed on custom-built mechanical models of the spine [26,53].
One study used the medimouse apparatus to compute   [50]. Only 1 study inserted wires into the vertebral body to quantify soft tissue artefact (STA) [68].

Suitability of the approach Marker setup
Most studies used clusters of single markers for their setups, only 7 studies used marker triads to define spine segments [38,53,55,68,72,83,88]. The spinous processes of C7, T3, T6, T12, L1, L3 and L5 were the most widely used. All studies reported marker positioning by palpation of the anatomical landmark surface. Two studies positioned markers following the curvature of the spine, at the points of most thoracic kyphosis and lumbar lordosis [23,64]. Information on the time needed to position the markers was not reported by any of the studies.
When it comes to the studies that recruited patients undergoing spine surgery [45,49,52,53,61,83], ADL tasks were used to assess improvement or deterioration of neurological symptoms, changes in motion patterns and the compensation mechanisms involved in the motion.
Patient considerations Studies involving patients and healthy subjects [12-14, 38-46, 52, 55, 59-61, 76, 79-81, 83, 86] had the same tasks for both cohorts. Participants were asked to perform their tasks at their self-selected speed. One study involving patients asked their participants to perform a lifting task only in their most comfortable approach [55].

Main measurements
Eighteen studies calculated the angles between the spine segments defined [23,26,42 The ROM of segments during walking tasks ranged from 2.3° to 7.9° in the sagittal plane, 1.8° to 10.8° in the frontal plan while most of the motion was recorded in the transverse plane ranging from 2.6° to 13.5°. Detailed ROMs of the spine segments defined in the studies extracted can be found in Table 7.
Four studies [63,71,73,76] reported the angle of inclination between the segments and as such calculated the angles of lumbar lordosis or thoracic kyphosis.
Of the 24 studies that conducted walking trials [
Six studies assessed patients undergoing spine surgery, 5 of them had patients who underwent posterior spinal fusion surgery [49,52,53,61,83] while 1 study had                          patients undergoing two different decompression surgery approaches [45]. Four studies assessed patient motion before and after surgery. One study measured patients before and 1 month after [45], another measured patients before, 3 months and 12 months after surgery [49], Patel et al. [61] measured patients before and 12 months following surgery while Konz et al. [53] analysed their subject before and 6 months after surgery.

Clinical findings
The studies including patients assessed the kinematics of the multi-segmental spine to help clinical decisions, provide more information on motion compensation, evaluate treatment, and monitor pathology outcome. Kuwahara et al. [45] used the multi-segmental motion approach to compare two decompression surgery techniques and measure the improvement of neurological symptoms following surgery of the two-patient cohort. Hemming et al. [43] found evidence to support subgrouping LBP patients to better refine intervention approaches. Christe et al. [14] suggested that CLBP patient rehabilitation could benefit from targeting specific motion deficits in functional activities.
Of the 29 studies assessing patients, 3 studies [40,41,61] reported motion asymmetry at the levels of the lumbar and thoracic spine between the patient and control cohorts, Christe et al. [41] reported a 20% increase in transverse plane asymmetry in CLBP patients (Table 7) while Patel et al. [61] reported asymmetric axial plane motion in LBP patients. 4 studies assessed spine rotation abilities depending on the pathology, 3 of these [12,41,42] reported up to 15% decrease in segment rotation either after a surgical intervention or due to LBP (Table 7). Only 1 study [79] reported an increase in lumbar and thoracic rotations in patients with LBP. The motion profile of axial spondylopathy patients was seen to be similar to the maladaptive motion profiles of patients with CLBP with a significant decrease in motion velocity when compared to controls [39].
When it comes to the motion of the lumbar spine, 3 studies reported a decrease in lumbar spine flexion in LBP patients [13,41,44] (Table 7), while 1 study [42] reported a decrease in lower lumbar flexion but an increase in upper lumbar flexion. One study [60] found an increase in the upper lumbar and lower lumbar ROM during walking, sit-to-stand and running tasks in patients with LBP (Table 7). Five studies reported the motion coordination present between the spinal segments [55,59,62,80,88]. Of these, two studies [59,80] found a lack of coordination between the lumbar and thoracic segments in LBP and AIS patients. One study [62] found that the pattern of coordination between segments is different for LBP patients when compared to the control and 1 study [55] found evidence of coordination between the upper lumbar, thoracic and pelvis to stabilize the trunk in ankylosing spondylitis patients. One study assessing the motion of rowers with CLBP [88] found a lack of coordination between the spinal segments when the intensity of the motion is increased while also finding that the lower spine segments could not work as supports for the upper segments.
Five studies [23,38,46,63,73] reported the changes in spine curvature during dynamic trials when compared to static posture. These were able to show that curvature angles of the spine could be measured with high accuracy and that regional differences exist depending on the pathology. One study [76] reported a decrease in the lumbar lordosis angle during walking and running in patients with non-specific LBP. Two studies [49,83] reported the motion of the spine following fusion surgery, one with AIS patients and the other with ASD patients, both did not report any hypermobility in the unfused spinal segment. Only one study [81] found no significant spine kinematic differences between the LBP group and the control group.

Discussion
Motion abnormalities of the spine impact the onset and recurrence of spinal disorders [11,12], therefore analysing the kinematics of the thoracolumbar spine gives an insight into the causes of these disorders and aids in the choice of treatment [13,14]. Stereophotogrammetric motion analysis could objectively quantify this motion [22,23], however numerous methods and protocols are found in the literature. The current review aims to evaluate these studies and assess their reliability, suitability in a clinical setting and clinical significance. Seventy-four articles were identified focusing on the multi-segmental motion of the thoracolumbar spine of which 44 articles proposed a different protocol to quantify this motion. These protocols differed in the number of markers used, segments defined, participant cohorts recruited, disorders analysed, kinematic variables assessed, and outcome measurements reported highlighting the need for a set of standard principles to provide reliable and reproducible kinematic information on various motions, spine segments and spine disorders.

Reliability of the motion capture setup
The reliability of the identified studies was first evaluated. It was defined as the repeatability and accuracy of the measurement approach in addition to the analysis of sources of error. Most studies did not report on these three reliability aspects scoring 32%, 18% and 18% respectively in the quality assessment questionnaire. To quantify the repeatability of the measurement, we first looked at task repetitions; most studies asked their participants to repeat the motion at least three times [12-14, 23, 26, 30, 39-44, 46, 47, 52-55, 58-62, 65-70, 72, 75, 76, 78, 80, 82, 83, 85, 89, 94, 95, 97] and ultimately based their measurements on the average of trials, however, the repetitions of tasks were unrelated to the number of participants in the cohorts. Some of the studies succeeded in analysing the repeatability of the outcome measurement either by studying the intra-subject variability [23,38,46,69,70,72,85,89,95,105], the inter-rater reliability [38,82,95] or the repeatability of the findings when measured across different days [26,30,38,82,91]. When it comes to the accuracy of the optoelectronic protocol, 11 studies [26,46,53,54,63,67,68,71,73,82,84] compared their results to more conventional imaging techniques to show the accuracy of the marker setup and their reported outcomes; however, the remaining studies did not report on these differences as they were investigating the changes in spine motion between cohorts and were not reporting the absolute angle of motion of spinal segments [12-14, 38, 40-46, 55, 59, 61, 79-81, 83]. Deane et al. [95] was the only study to quantify the standard error associated with spine motion ranging between 0.8° and 5.5° for gait and between 1° and 12.6° for sit-to-stand motion compared to imaging techniques that account for a < 1° of error during static measurements [19]. Only 9 studies [38,40,50,53,66,73,84,87,94] reported the marker placement error associated with the setup, this is especially important as the spine region is greatly affected by STA [72] and hence would be expected to be more thoroughly reported. None of the studies identified in this review however was found to report on all three reliability aspects assessed in the quality questionnaire. These shortcomings affect the reliability of the protocols suggested and make implementing a standard protocol in a clinical setting even more difficult.

Suitability of the approach
When assessing the suitability of the protocols suggested for a clinical setting, we looked at marker configurations, segment definitions, participant cohorts, tasks conducted outcome measures and the ease of use of the methodology in a clinical setting. Major differences in marker setups were seen across studies, with different numbers of markers on the thoracolumbar spine and their location on the anatomical landmarks; the most common anatomical landmarks to attach the markers on were C7/ T1, T6/T7, T12/L1, L3, L5. Only 11 studies [23,30,46,52,56,71,73,76,[85][86][87] reported positioning of markers anteriorly to the spine on the sternum to decrease the effect of STA on the measurement while the majority of the studies positioned markers laterally to the spine [13,14,40,41,45,48,57,58,62,63,65,66,77,81,82,88,89,94,96]. Some of these marker setups were seen to be very complex for a clinical setting and are more suited for research purposes as they require more time to position due to the high number of marker [38,46,50,51,55,56,67,68,73,79,80,88,90,91], other studies [12-14, 23, 39, 41-44, 57-59, 64-66, 75, 81, 92, 94, 97] were seen to be successful in limiting the number of markers on the spine or by using 3D clusters. This limitation was mentioned by Glover et al., [87], who saw that a higher number of markers on the spine decreases marker tracking error but the implementation of the protocol and processing the data would take a significantly longer time. A poor consistency was found in terms of thoracolumbar segment definition. These changed depending on the study cohorts and tasks of interest. The majority of studies tried to define at least the thoracic and lumbar spines [30, 45, 48, 49, 56, 61-63, 71, 74, 78, 83-86], the lumbar spine was further divided into upper and lower segments [12-14, 41-44, 59, 60, 81, 90, 94, 97] especially when investigating patients with LBP due to the changes in motion seen at each level [12,42,43,59,60,90]. The thoracic spine was also divided into upper and lower segments to have a better understanding of the less studied kinematics of the thoracic spine and help in the investigation of kyphotic and scoliotic spines [13,14,23,41,50,56,81,90]. When it comes to participant considerations, most of the studies tried to match the age of participants with only 9 studies including participants with an age range difference exceeding 10 years [38,39,43,45,47,55,75,79,94]. More than half of the studies investigated ADLs such as lifting, sit-to-stand, stair climbing and walking. These tasks had been seen to present a challenge to spine pathology patients and could highlight the differences in segment ROM and coordination when compared to controls [13,14,23,31,41]. The angle between the defined segment was the main outcome reported by studies independent of the tasks conducted, marker setup used, or segments defined. Despite ROM being a straightforward indication of motion ability and is easily estimated even in a clinical setting, it can limit our understanding of motion contribution, compensation mechanisms and coordination between the spine segments [31]. The coordination between the segments wasn't as widely reported although evidence has been found to show changes in coordination due to age and spine pathology [55,59,62,80,88]. None of the studies in this review reported on the time needed for each measurement or the ease of use of their processing approach in a clinical setting. Hence after assessing the suitability of the studies found, ADLs remain the most useful tasks to understand spine motion and its pathologies [13,14,23,31,41] while more investigations are needed to agree on marker setups and segments definitions to be used in a clinical setting in addition to what to report when it comes to outcome measurements.

Clinical significance
When it comes to the clinical significance of the studies evaluated, this was defined as the relevancy of the study and its outcome measurements to a certain spine pathology. Different kinematic findings were reported by the studies depending on the spine pathology, the multi-segmental approach and the marker setup used. When considered as one moving segment, the lumbar spine flexion was seen to decrease overall in subjects with LBP [13,41,44]; however, when further dividing the lumbar spine into upper and lower segments, motion contribution by the UL was seen to be greater than the LL segment [12,42]. As such, segment definition plays a key role in understanding the effects of pathology on spine motion; it is advised to divide the spine into more than 2 segments to be able to describe the motion of the whole spine and understand the contribution of each segment [46]. Besides, grouping patients into subcategories depending on their motion impairments [43] or surgical treatments [45] could reveal the similarities in the kinematic findings against healthy controls [31]. Considerations for the changes in spine motion due to age were limited. Only 2 studies reported the differences in spine ROM between older and younger adults [50,51] while the majority of the studies reported the motion of the spine in healthy younger adults under the age of 35 [23, 47, 48, 53, 56-58, 65-67, 71, 72, 77, 78, 82, 89, 93, 95-97]. Significant age-related lumbar segment reductions in motions have however been reported in the literature [32], it is therefore advised to investigate the spine motion of both older and younger adults and spine pathology subjects to define the motions of each segment of the spine and the coordination between the segments. When looking at the differences between patients and controls, distinct motion perturbations were found in the axial and sagittal plane during spine motion in addition to transverse plane asymmetry in subjects with spine pathologies [12-14, 39-42, 44, 79, 80, 88]. Hence it is advised to investigate the motion of the defined segments in the three dimensions of motion in addition to studying the coordination between spine segments and to the pelvis to ultimately define distinct motion characteristics for LBP, AIS, ASD or spine surgery patients. The use of a multi-segmental spine motion protocol was seen to be successful in a clinical setting to accurately assess spine curvature [23,38,46,63,73] and the effect of surgical treatment on the patient motion [45,49,83]. Evidence has been found in this review to support the use of a multi-segmental approach for spine motion analysis to help clinicians in the diagnosis and treatment of spine disorders.

Limitations
The present study has a few limitations. Only three research databases were queried for articles published in a peer-reviewed journal and only in English. Hence, a publication or language bias might have occurred. The quality assessment questionnaire developed was not assessed for objective reliability and validity although it was constructed using prior assessments found in the literature [31,37]. A reliability assessment of the extracted data and the quality assessment questionnaire was not carried out as they were completed by only one reviewer. The review only included studies using passive markers and an optoelectronic system. Studies assessing multi-segmental spine motion using inertial markers or wearable technology were not assessed due to the high signal to nose ratio linked to these sensors especially when attached to a vertebral landmark [65]. Additionally, studies assessing only the motion of the cervical spine were not included as only the motion of the thoracolumbar spine was found to be relevant to the onset of LBP and ASD [1,35].

Conclusions
The current review showed a shortage in standard protocols to assess spine motion using optoelectronic techniques to identify and support clinical investigations. The findings mentioned in the review could be used when trying to choose the most fitting protocol to assess the motion of the thoracic and lumbar spines. Based on the studies assessed in the review, separating each of the thoracic and lumbar segments into upper and lower parts is essential to accurately describe the motion of the spine. Markers attached to C7/T1, T6/T7, T12/L1, L3, L5 in addition to anterior markers on the sternum are needed to describe this motion. This limited number of markers would allow for easier application in a clinical setting. In terms of instrumentation, a motion analysis system made up of at least 6 cameras is needed. However, no study in this review mentioned the cost incurred by such an analysis and a cost effectiveness study would need to be completed to assess the feasibility of using spine motion analysis in a clinical setting. Additionally standardizing the marker setups, segment definitions and tasks conducted as part of a multicentric study could prove to help identify more accurate clinical applications for spine motion analysis.